Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia

Soil-borne pathogens cause high losses in crop yields globally. The development of environmentally friendly approaches is urgently needed, but is often constrained by complex interactions between root-associated microbes and pathogens. Here, we demonstrate that the interactions within microbial cons...

Full description

Bibliographic Details
Main Authors: Shaohua Gu, Tianjie Yang, Zhengying Shao, Tao Wang, Kehao Cao, Alexandre Jousset, Ville-Petri Friman, Cyrus Mallon, Xinlan Mei, Zhong Wei, Yangchun Xu, Qirong Shen, Thomas Pommier
Format: Article
Language:English
Published: American Society for Microbiology 2020-06-01
Series:mSystems
Subjects:
Online Access:https://doi.org/10.1128/mSystems.00811-19
id doaj-bbd26a6074e242a090dacba1fea75129
record_format Article
spelling doaj-bbd26a6074e242a090dacba1fea751292020-11-25T03:18:42ZengAmerican Society for MicrobiologymSystems2379-50772020-06-0153e00811-1910.1128/mSystems.00811-19Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial ConsortiaShaohua GuTianjie YangZhengying ShaoTao WangKehao CaoAlexandre JoussetVille-Petri FrimanCyrus MallonXinlan MeiZhong WeiYangchun XuQirong ShenThomas PommierSoil-borne pathogens cause high losses in crop yields globally. The development of environmentally friendly approaches is urgently needed, but is often constrained by complex interactions between root-associated microbes and pathogens. Here, we demonstrate that the interactions within microbial consortia mediated by iron-scavenging siderophores play an important role in reducing pathogen infection and enhancing plant health. This study provides a promising and novel research direction for dealing with a wide range of microbial infections through iron exploitation, which is important for the colonization and infection of both plant and human hosts by pathogens.Interactions between plant pathogens and root-associated microbes play an important role in determining disease outcomes. While several studies have suggested that steering these interactions may improve plant health, such approaches have remained challenging in practice. Because of low iron availability in most soils, competition for iron via secreted siderophore molecules might influence microbial interaction outcomes. Here, we tested if bacterial interactions mediated by iron-scavenging siderophores can be used to predict the disease suppressiveness of microbial consortia against soilborne Ralstonia solanacearum, a bacterial pathogen in the tomato rhizosphere. Iron availability significantly affected the interactions within inoculated consortia and between the consortia and the pathogen. We observed contrasting effects of siderophores and other nonsiderophore metabolites on the pathogen growth, while the siderophore effects were relatively much stronger. Specifically, disease incidence was reduced in vivo when the inoculated consortia produced siderophores that the pathogen could not use for its own growth. Employing siderophore-mediated interactions to engineer functionally robust microbial inoculants shows promise in protecting plants from soilborne pathogens.https://doi.org/10.1128/mSystems.00811-19siderophoremicrobial interactionsplant healthplant pathogenssoil microbiology
collection DOAJ
language English
format Article
sources DOAJ
author Shaohua Gu
Tianjie Yang
Zhengying Shao
Tao Wang
Kehao Cao
Alexandre Jousset
Ville-Petri Friman
Cyrus Mallon
Xinlan Mei
Zhong Wei
Yangchun Xu
Qirong Shen
Thomas Pommier
spellingShingle Shaohua Gu
Tianjie Yang
Zhengying Shao
Tao Wang
Kehao Cao
Alexandre Jousset
Ville-Petri Friman
Cyrus Mallon
Xinlan Mei
Zhong Wei
Yangchun Xu
Qirong Shen
Thomas Pommier
Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
mSystems
siderophore
microbial interactions
plant health
plant pathogens
soil microbiology
author_facet Shaohua Gu
Tianjie Yang
Zhengying Shao
Tao Wang
Kehao Cao
Alexandre Jousset
Ville-Petri Friman
Cyrus Mallon
Xinlan Mei
Zhong Wei
Yangchun Xu
Qirong Shen
Thomas Pommier
author_sort Shaohua Gu
title Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
title_short Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
title_full Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
title_fullStr Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
title_full_unstemmed Siderophore-Mediated Interactions Determine the Disease Suppressiveness of Microbial Consortia
title_sort siderophore-mediated interactions determine the disease suppressiveness of microbial consortia
publisher American Society for Microbiology
series mSystems
issn 2379-5077
publishDate 2020-06-01
description Soil-borne pathogens cause high losses in crop yields globally. The development of environmentally friendly approaches is urgently needed, but is often constrained by complex interactions between root-associated microbes and pathogens. Here, we demonstrate that the interactions within microbial consortia mediated by iron-scavenging siderophores play an important role in reducing pathogen infection and enhancing plant health. This study provides a promising and novel research direction for dealing with a wide range of microbial infections through iron exploitation, which is important for the colonization and infection of both plant and human hosts by pathogens.Interactions between plant pathogens and root-associated microbes play an important role in determining disease outcomes. While several studies have suggested that steering these interactions may improve plant health, such approaches have remained challenging in practice. Because of low iron availability in most soils, competition for iron via secreted siderophore molecules might influence microbial interaction outcomes. Here, we tested if bacterial interactions mediated by iron-scavenging siderophores can be used to predict the disease suppressiveness of microbial consortia against soilborne Ralstonia solanacearum, a bacterial pathogen in the tomato rhizosphere. Iron availability significantly affected the interactions within inoculated consortia and between the consortia and the pathogen. We observed contrasting effects of siderophores and other nonsiderophore metabolites on the pathogen growth, while the siderophore effects were relatively much stronger. Specifically, disease incidence was reduced in vivo when the inoculated consortia produced siderophores that the pathogen could not use for its own growth. Employing siderophore-mediated interactions to engineer functionally robust microbial inoculants shows promise in protecting plants from soilborne pathogens.
topic siderophore
microbial interactions
plant health
plant pathogens
soil microbiology
url https://doi.org/10.1128/mSystems.00811-19
work_keys_str_mv AT shaohuagu siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT tianjieyang siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT zhengyingshao siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT taowang siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT kehaocao siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT alexandrejousset siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT villepetrifriman siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT cyrusmallon siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT xinlanmei siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT zhongwei siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT yangchunxu siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT qirongshen siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
AT thomaspommier siderophoremediatedinteractionsdeterminethediseasesuppressivenessofmicrobialconsortia
_version_ 1715251412222345216